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Review

Interstitial Telomeric-like Repeats (ITR) in Seed Plants as Assessed by Molecular Cytogenetic Techniques: A Review

by
Alexis J. Maravilla
,
Marcela Rosato
and
Josep A. Rosselló
*
Jardín Botánico, ICBiBE, Universitat de València, c/Quart 80, E-46008 València, Spain
*
Author to whom correspondence should be addressed.
Plants 2021, 10(11), 2541; https://doi.org/10.3390/plants10112541
Submission received: 18 October 2021 / Revised: 11 November 2021 / Accepted: 16 November 2021 / Published: 22 November 2021
(This article belongs to the Special Issue Plant Evolutionary Cytogenetics)
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Abstract

:
The discovery of telomeric repeats in interstitial regions of plant chromosomes (ITRs) through molecular cytogenetic techniques was achieved several decades ago. However, the information is scattered and has not been critically evaluated from an evolutionary perspective. Based on the analysis of currently available data, it is shown that ITRs are widespread in major evolutionary lineages sampled. However, their presence has been detected in only 45.6% of the analysed families, 26.7% of the sampled genera, and in 23.8% of the studied species. The number of ITR sites greatly varies among congeneric species and higher taxonomic units, and range from one to 72 signals. ITR signals mostly occurs as homozygous loci in most species, however, odd numbers of ITR sites reflecting a hemizygous state have been reported in both gymnosperm and angiosperm groups. Overall, the presence of ITRs appears to be poor predictors of phylogenetic and taxonomic relatedness at most hierarchical levels. The presence of ITRs and the number of sites are not significantly associated to the number of chromosomes. The longitudinal distribution of ITR sites along the chromosome arms indicates that more than half of the ITR presences are between proximal and terminal locations (49.5%), followed by proximal (29.0%) and centromeric (21.5%) arm regions. Intraspecific variation concerning ITR site number, chromosomal locations, and the differential presence on homologous chromosome pairs has been reported in unrelated groups, even at the population level. This hypervariability and dynamism may have likely been overlooked in many lineages due to the very low sample sizes often used in cytogenetic studies.

1. Introduction

The physical package of genetic material is organised in universal structures called chromosomes. In prokaryotes, and in the organelles, chromosomes display a single and circular structure in the absence of a surrounding membrane envelope. However, in the nucleus of most eukaryotes, chromosomes are linear, and their numbers, shape, size, and C-genome size vary greatly among species.
Structurally, a canonical eukaryote chromosome consists basically of chromatids, a centromere, and telomeres, which are preserved during cell division through mitosis and meiosis. Centromeres and telomeres are vital for the integrity of eukaryotic chromosomes. The former play a key role in the precise segregation of chromosomes throughout mitosis and meiosis processes during cell divisions. Meanwhile, telomeres are the terminal DNA-nucleoprotein complexes of chromosomes (Figure 1A), capping their ends and protecting the chromosome against end-to-end fusions [1].
Interstitial telomeric repeat (ITR) sites, also known as interstitial telomeric sequences (ITSs), consist of tandem repeats of telomeric motifs that are located within intrachromosomal regions (Figure 1B), including repeats located close to the centromeres and the ones found between the centromeres and the telomeres [2].
Their presence in fungi [3], vertebrates [4,5], and plants [6,7,8,9,10] suggests that (1) the acquisition of telomeric repeats inside chromosomes in unrelated organisms is a convergent event during karyotype evolution, and (2) multiple cytogenetic and molecular mechanisms might have contributed to the diversity of their formation.
Discovering telomeric repeats in interstitial regions of plant chromosomes using molecular cytogenetic techniques was achieved several decades ago [11], and many subsequent reports have been published to date e.g., [12]. Their study has revealed the perception that they are relevant and stable karyological landmarks. However, the information is scattered and has not been critically evaluated from an evolutionary perspective. To fill these gaps, we have critically reviewed the available information related to ITRs on seed plants as assessed by molecular cytogenetic methods. Based on the currently available data, these karyological landmarks are evaluated by (1) detecting emerging patterns of variation in presence and site number across major evolutionary lineages and at several hierarchical levels, (2) assessing the possible associations between the occurrence, number and chromosomal location of ITR sites and the chromosome number of the analysed species, (3) estimating the utility of ITRs as phylogenetic and taxonomic markers in plants, (4) discussing the main mechanisms involved in the genesis of ITRs, and (5) assessing the role of biological processes that may have triggered the evolution of ITRs in seed plants.

2. Molecular Cytogenetic Approaches Used in ITR Detection

In situ hybridisation (ISH) techniques have become one of the most powerful approaches for mapping specific sequences of DNA in plant cytogenetics, including telomere sequences. The basic principles underlying ISH is similar among all the types of experimental variants that have been developed, regardless of whether standard or sophisticated methods were used. However, experimental issues involving the type of the used probes (cloned, synthetic oligonucleotides), probe labeling (nick-translation, PCR-labeling, pre-labeled oligomer), and probe detection (fluorescent, enzymatic) contribute to the sensitivity of ISH approaches [13,14,15,16]. Several technical approaches have been used to date to detect telomeric repeats in plants, including non-Isotopic ISH [11], FISH (fluorescent in situ hybridisation; [6]), PRINS (primer in situ DNA labeling, [17]), PNA-FISH (peptide nucleic acid-FISH, [18]), ND-FISH (non-denaturant-FISH, [19]), PLOPs-FISH (Pre-Labelled Oligomer Probes, [16]), and CO-FISH (chromosome orientation-FISH, [20]). The drawback of molecular cytogenetic methods is that short arrays of telomeric-like sites may be undetectable by ISH [21]. In these cases, DNA sequencing of interstitial chromosomal regions or whole genomes is the best available option [22].
Initially, the location of telomeres in plant chromosomes were identified in Hordeum vulgare and Secale cereale by [11], who also detected interstitial sites. Some years later, a synthetic oligonucleotide (TTTAGGG), representing the canonical Arabidopsis-type repeat was used as a template in PCR and fluorescently labelled to locate telomere repeats in several unrelated flowering plant species [6]. Most of the studies (71.56%) dealing with the cytogenetic mapping of plant telomeres used synthetic oligonucleotide probes for ISH, including the Arabidopsis-type repeat (53.13%; e.g., [7]), the vertebrate-type repeat (TTAGGG) (15.62%; e.g., [23]), other unusual plant-specific telomere sequences (CTCGGTTATGG, TTTTTTAGGG, T4-5AGCA, TTCAGG and TTTCAGG; 2.14%, e.g., [24,25,26,27]), and the Tetrahymena-type repeat (TTGGGG; 0.67%, e.g., [23]), while a significantly lower number (28.44%) used cloned sequences involving the Arabidopsis clone (27.90%; e.g., [28]) or other specific telomeric regions (0.54%; e.g., [18]). The most likely reasons explaining the preferential use of synthetic probes over cloned sequences may be related to the more complex technical requirements and higher costs involved in the handling and conservation of clones. Currently, ITR repeats detected in plants are constituted by the Arabidopsis-type (TTTAGGG), vertebrate-type (TTAGGG), and Cestrum-type (T4-5AGCA) sequences.

3. ITR Sampling in Seed Plants

A total 627 species from 330 genera belonging to 79 families (sensu APG IV) have been karyologically analysed to detect telomeric sequences in seed plants [6,7,8,10,11,12,16,17,18,19,20,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184,185]. These figures sharply contrast with the greater amount of data reported for nuclear ribosomal DNA loci (35S and 5S rDNA families), the most popular chromosomal landmarks used in plant molecular cytogenetics, with data available for 2148 species, 540 genera, and 114 families [186].
The sampling for detecting telomeric sequences is uneven and biased towards the analysis of large groups, with some exceptions (Figure 2).
Whereas in gymnosperms there is a lack of data only for Gnetales, in angiosperms the number of major groups analysed (11) nearly equals those for which there is no data (13). Speciose ordinal groups not sampled to date are few and include Proteales, Vitales, Santalales, and Cornales, which encompass between 14–151 genera and 590–1750 species [187]. Unfortunately, no species from the three most basal lineages of angiosperms (Amboreallales, Nymphaeales, Austrobaileyales) have been analysed. Although the overall diversity of these orders is fairly limited (12 genera and about 175 species; [187]), their key position in the ancestral diversification of flowering plants makes them priority targets for assessing the presence of ITRs.
Plants 10 02541 g002 550
Figure 2. Occurrence of ITR sites in seed plants. The absence (grey colour) and presence (orange colour) in major lineages is illustrated. Unsampled groups are depicted in white. The overview of the phylogenetic relationships is based on [188] for Gymnosperms and [189] for Angiosperms.
Figure 2. Occurrence of ITR sites in seed plants. The absence (grey colour) and presence (orange colour) in major lineages is illustrated. Unsampled groups are depicted in white. The overview of the phylogenetic relationships is based on [188] for Gymnosperms and [189] for Angiosperms.
Plants 10 02541 g002

4. Taxonomic Distribution of ITRs Is Widespread among Major Lineages of Seed Plants

With the exception of Chloranthales, which exhibits a scarce diversity and has only had three of its analysed, and the monotypic Ginkgoales, all major evolutionary groups sampled had ITRs in their karyotypes (Figure 2 and Figure 3).
However, heterogeneity regarding the distribution at lower taxonomic units is noteworthy. Thus, ITRs occur in only 36 out of 79 sampled families (45.57%), suggesting that disparate results occur within major plant lineages. In gymnosperms, the families with the higher number of ITR occurrences are Podocarpaceae (8 spp.) and Pinaceae (6 spp.), whereas Asteraceae (37 spp.), Fabaceae (21 spp.), and Poaceae (8 spp.) lead among angiosperms. It should be stressed, however, that due to the uneven sampling effort made at different taxonomic levels, these results could be skewed and may not reflect the real values. In this regard, it is worth mentioning that at the family level, the number of species showing ITRs in their karyotypes is strongly correlated to the number of sampled species (Pearson correlation value = 0.994, p < 0.0001).
Overall, lower and similar frequencies of occurrence are attained at the generic and species level. ITRs have been detected in only 88 out of 330 analysed genera (26.67%) and in 149 out of 627 sampled species (23.73%). These results clearly show that although ITRs are widespread in seed plants, their frequency at low taxonomic units is fairly moderate.

5. ITRs Preferentially Occur at Interstitial Chromosomal Arms

The longitudinal distribution of ITR sites along the chromosome arms is uneven (Table 1). Overall, more than half of the ITRs occur between proximal and terminal locations (49.5%), followed by proximal (29.0%) and centromeric (21.5%) arm regions. Interestingly, the relative order of occurrence contrasts between gymnosperms and angiosperms. The former shows higher occurrences at centromeric locations whereas proximal locations are more abundant in angiosperms (Figure 4).
Within gymnosperms there are several contrasting trends for Pinales and Cupressales orders (Figure 4). No centromeric ITR signals have been reported for the latter and most occurrences are at interstitial sites. Dissimilar values are reported for Pinales, where nearly equivalent occurrences at interstitial, proximal, and centromeric regions are reported. In angiosperms, the three major lineages with the highest number of species with ITRs (Monocots, Fabids and Campanulids) do not show clear divergent patterns related to the longitudinal distribution of ITR sites along the chromosome arms (Figure 3).

6. The Number of ITR Sites Greatly Varies among Congeneric Species and Higher Taxonomic Units

There is a wide range of reported ITR signals, from one (Gibasis pulchella, Comme-linaceae, [6]) to 72 signals (Pinus taeda, Pinaceae; [35]), although a high but undetermined number reported in the monocot Anthurium wendlingeri [84] may eventually exceed the later value. ITR signals mostly occur as homozygous loci in most species. However, odd numbers of ITR sites reflecting a hemizygous state have been reported in both gymnosperm and angiosperm groups. Hemizygosity in the former is restricted to Cycadales (Cycas revoluta [30]. Interestingly, Cycas revoluta is a dioicous species, and Hizume et al. [30] indicated that hemizygosity was associated with the heteromorphic sexual chromosome pair. Thus, male plants showed an odd number of ITR signals when compared to females, providing additional cytogenetic markers to characterize sexual chromosomes in this species. The differential association of ITR sites and sexual chromosomes has not been reported in other species of Cycadales which have male and female individuals [37,38]. Unfortunately, neither the number of individuals analysed nor the gender of their accessions were specified [37,38]. This casts doubt on whether ITRs are involved in the genomic evolution of the sexual chromosomes in Cycadales.
Greater hemizygosity is present in angiosperms (16 species), including Campanulids (nine species), Monocots (four species), Fabids (two species), and Caryophyllales (one species). All sampled species are hermaphrodite or monoicous and the odd numbers of ITR are not related to any obvious biological trait.
The overall average number of sites in species where ITRs have been reported is 10.33 ± 13.36. However, when the values are separately calculated for gymnosperms and angiosperms, the data strongly differ. Gymnosperm species show an average of 32.60 ± 24.53 sites in contrast with the exceedingly low value of 7.82 ± 8.50 obtained from angiosperms. Moreover, there are also diverging values in ITR site numbers among major lineages of seed plants. This has been clearly revealed in groups where a substantial number of species showing ITRs have been reported, e.g., Monocots, Fabids, Lamids, and Campanulids (Figure 5).
Congeneric species may differ in the presence or absence of ITR signals as observed in unrelated groups from 16 families. This is illustrated in Asteraceae, where intrageneric polymorphisms have been detected in Achillea, Anacyclus, Anthemis, Cladanthus, Nassauvia, and Sonchus [69,82], Alstroemeriaceae (Alstroemeria, [31,44]), Brassicaceae (Brassica, [60]), Solanaceae (Cestrum, [26,87]), Rutaceae (Citrus, [92,93]), Poaceae (Colpodium, Hordeum, [47,61,94,95]), Cucurbitaceae (Cucumis, [98,99]), Orchidaceae (Dendrobium, [41]), Cyperaceae (Eleocharis, [48,97]), Lentibulariaceae (Genlisea, [27]), Cannabaceae (Humulus, [100,101]), Juncaceae (Luzula, [96]), Amaryllidaceae (Nothoscordum, Prospero, [18,23,86]), Rosaceae (Rosa, [62,103]), Fabaceae (Senna, Vicia, [7,45,74]), and Commelinaceae (Tradescantia, [6,103]).

7. Variable Presence and Location of ITR Sites Occur within Species

Intraspecific variation regarding the presence and absence of ITR signals has been reported in a relatively low number of specie: the gymnosperm Zamia furfuracea (Zamiaceae, [7,37]) and the angiosperms Beta vulgaris (Amaranthaceae, [7,104]), Brassica oleracea (Brassicaceae [60,102]), Cestrum parqui (Solanaceae, [26,87]), Hordeum vulgare (Poaceae, [6,11]), Humulus scandens (Cannabaceae, [56,100]), Luzula luzuloides (Poaceae, [7,96]) Vicia faba (Fabaceae, [7,45]), Solanum tuberosum (Solanaceae, [7,31]), Sonchus tenerrimus (Asteraceae, [69]), Tanacetum parthenium (Asteraceae, [69,103]) and three species of Anacyclus (Asteraceae), A. clavatus, A. monanthos and A. valentinus [82].
Moreover, additional intraspecific polymorphisms involving contrasting chromosomal locations and a differential presence of the ITR sites on homologous chromosome pairs have been also reported. The most extreme case documented thus far occurs in Anacyclus (Asteraceae), where intraspecific hypervariability and dynamism was documented in six of the nine known species of the genus, using a large sampling size [82]. The extent of the variation was so high that all analysed individuals showing ITRs could be distinguished by their cytogenetic patterns [82]. Such remarkably high levels of polymorphism, indicating that ITRs are a labile genomic feature within a single species, were unnoticed and not previously reported in plants. An issue in need of additional research is to assess whether Anacyclus is an isolated case of ITR dynamism in seed plants or if this pattern might have been overlooked in other unrelated groups due to the low sample sizes often used in cytogenetic studies.

8. The Presence of ITRs and the Number of Sites Is not Significantly Related to Number of Chromosomes

Overall, no apparent association was detected between the presence of ITR signals and the number of chromosome of the analysed species (Pearson correlation value r = −0.130, p < 0.001). This lack of association was also reported when analysing partial but significant datasets. Thus, for Asteraceae (by far the most sampled family of seed plants), the correlation value between these two parameters is close to 0 [69].
ITRs were detected in all haploid chromosomal intervals from n = 2–5 up to n = 36–40, albeit with contrasting values (Figure 6).
The existence of ITRs has not been documented in species showing a haploid chromosome number higher than n = 41. The maximum presence of species showing ITRs falls within chromosome interval n = 6–10. The latter results should be interpreted with caution and probably have no underlying evolutionary significance. A close dissection of the data indicates that 39.4% of the species from the n = 6–10 range showing ITRs belong to the Asteraceae where the highest presence of ITRs occurs in species with n = 9 chromosomes [69].
As a rule, few species with a chromosome number n = 21 or higher have been reported to show ITRs. However, it should be noted that this trend may be another result of the sampling since very few species with high chromosome numbers have been analysed.
Similarly, no significant association is detected between the total ITR sites present in the chromosome complement and the chromosome number (Pearson correlation value r = 0.031, p = 0.6745). This is clearly evidenced in Asteraceae, where species sharing the same number of chromosomes (2n = 18) showed a wide range of ITR sites (range = 2–52; [69]). Almost all fundamental lineages of seed plants have experienced episodes of whole-genome duplication events [190]. The recurrent cycles of paleo-polyploidisation have been followed by massive genomic and chromosome rearrangements resulting in losses, amplifications, translocations and inversions of DNA fragments thereby modifying genome architecture and ancestral chromosome numbers [191,192]. These complex and ancient evolutionary scenarios might compromise the right interpretation of karyotype changes and hypotheses on chromosomal number evolution, explaining the lack of positive correlation between ITRs and chromosome number.

9. Origin of ITRs

Since the initial identification in plant karyotypes it was suggested that ITRs could be considered cytological landmarks of chromosomal rearrangements [7]. It has been hypothesised that the presence of ITRs in the centromeric and peri-centromeric regions illustrate could be vestiges of ancestral end-to-end fusion events between non-homologous chromosomes that caused descendent dysploidy [84,85,193,194,195]. However, the presence of ITRs could also be explained by chromosome translocation and inversion mechanisms [196]. Thus, translocation-based descending dysploidy associated to the occurrence of ITRs has been suggested in Brassicaceae [197], and the presence of ITRs in Phaseolus microcarpus may be generated through pericentric inversions [185]. Another possible causal mechanism based on the heterochomatin distribution model [198] is the equilocal dispersion of telomeric DNA to interstitial regions of the chromosome via transposition or heterologous recombination [86].
Telomeric sequences are in fact a type of microsatellite repeats regarding their length, high number of copies, and their disposition in tandem arrays in the genome. This way, the amplification of telomere repeats could be generated through similar mechanisms involved in the genomic evolutionary dynamics of the satellite DNA [199]. The rapid turnover of satellite DNA and the amplification of long stretches of repetitive sequences could be explained by a mechanism of rolling-circle replication of extrachromosomal circular DNA (eccDNA) [200,201]. In fact, it has been suggested that eccDNA could be involved in the occurrence and amplification of megabase-sized ITRs in Solanum [58] and the hypervariable ITR distribution in Anacyclus species [82]. Alternatively, the repair mechanisms of DNA double-strand breaks could also help explain the presence of short stretches of ITRs [2]. The above mechanisms are not mutually exclusive and might act jointly to achieve the evolutionary turnover of plant ITRs. The diversity of processes likely involved in the origin of ITRs illustrates the need for caution when assessing their role in karyological evolution, genome divergence, and the evolutionary history of plants.

10. Data Analysis

Relevant information was retrieved regarding the number of chromosomes, karyotype description, presence or absence of ITRs, their location on chromosome arms, the type of telomeric repeat and methodological approach, if available. When possible, it was produced from the raw data obtained from published research. Species showing ITRs were further analysed and the number of sites and their location along the chromosome were recorded. The chromosome arm was divided into three major domains of unequal size, i.e., centromeric (c), proximal (p), and interstitial (i); and the location of ITR sites was mapped on these chromosomal regions. Basically, this distinction is based on [202], except that no distinction was made between the interstitial-proximal and interstitial-terminal regions. In the case of holokinetic chromosomes, ITR signals were arbitrarily classified as interstitials. The detailed distribution of ITRs in each of the two chromosome arms was usually not provided or listed in the original publications. Accordingly, the locations of ITRs in each chromosome were pooled regardless of being present in the short or long arm. Species lacking detailed information regarding the precise number of ITR sites or their chromosomal distribution were not taken into account in the numerical analyses concerning these parameters.
The current scientific name and authorships of the species covered in this paper were retrieved from [203]. The circumscription of the families and higher taxonomic lineages (orders) of seed plants follows the hypothesis of the Angiosperm Phylogeny Website [187]. The overview of the phylogenetic relationships among seed plants is based on [188] for Gymnosperms and [189] for Angiosperms. The information was connected in a single phylogenetic tree to map the presence of ITR data in an evolutionary context (Figure 1).

11. Conclusions

The detection of ITR sites using molecular cytogenetic techniques has provided relevant, but still limited, knowledge on the patterns and processes of plant evolution. The uneven taxonomic sampling performed to date is a major concern for obtaining a stable overall perspective on ITR evolution. Many lineages of angiosperms have not been analysed to assess the presence of ITRs. This is unfortunate, since there is a lack of data for critical groups, especially flowering plants, which are of paramount importance for assessing solid inferences about the ancestral states of ITRs in seed plants.
Establishing the evolutionary trends in ITR evolution is further complicated by the emerging view that these telomeric sequences may show a remarkable intraspecific dynamism, even at the population level, involving site number, chromosomal locations and the differential presence of the ITR site on homologous chromosome pairs. In the absence of suitable and hierarchical sampling sizes (individuals, populations and species), this hypervariability and dynamism may have likely been overlooked in many groups. Unfortunately, most data available on plants are based on the unsatisfactorily low sample sizes commonly used in cytogenetic studies. The contention that ITRs are, contrary to previous hypotheses, a labile genomic feature within a species, may severely restrict their use as phylogenetic and taxonomic markers in plants. On the contrary, it may open new ways for applying ITRs as useful karyological markers at the population level, providing enough information to identify plant individuals and trace micro-evolutionary events.

Author Contributions

Conceptualization, J.A.R.; methodology, A.J.M. and M.R.; formal analysis, A.J.M. and M.R.; data curation, A.J.M. and M.R.; writing—original draft preparation, J.A.R.; writing—review and editing, A.J.M., M.R., and J.A.R.; supervision, J.A.R.; funding acquisition, J.A.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partly funded by grants from the Spanish Ministry of Economy and Competitiveness through the projects CGL2013-49097-C2-1-P and CGL2017-88500-P.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Nelson, A.D.; Beilstein, M.A.; Shippen, D.E. Plant telomeres and telomerase. In Molecular Biology; Howell, S.H., Ed.; Springer: New York, NY, USA, 2014; pp. 25–49. [Google Scholar]
  2. Lin, K.W.; Yan, J. Endings in the middle: Current knowledge of interstitial telomeric sequences. Mutat. Res. 2008, 658, 95–110. [Google Scholar] [CrossRef] [PubMed]
  3. Aksenova, A.Y.; Greenwell, P.W.; Dominska, M.; Shishkin, A.A.; Kim, J.C.; Petes, T.D.; Mirkin, S.M. Genome rearrangements caused by interstitial telomeric sequences in yeast. Proc. Natl. Acad. Sci. USA 2013, 110, 19866–19871. [Google Scholar] [CrossRef] [Green Version]
  4. Ocalewicz, K. Telomeres in fishes. Cytogenet. Genome Res. 2013, 141, 114–125. [Google Scholar] [CrossRef]
  5. Bolzán, A.D. Interstitial telomeric sequences in vertebrate chromosomes: Origin, function, instability and evolution. Mutat. Res./Rev. Mutat. Res. 2017, 773, 51–65. [Google Scholar] [CrossRef] [PubMed]
  6. Cox, A.V.; Bennett, S.T.; Parokonny, A.S.; Kenton, A.; Callimassia, M.A.; Bennett, M.D. Comparison of plant telomere locations using a PCR-generated synthetic probe. Ann. Bot. 1993, 72, 239–247. [Google Scholar] [CrossRef]
  7. Fuchs, J.; Brandes, A.; Schubert, I. Telomere sequence localization and karyotype evolution in higher plants. Plant Syst. Evol. 1995, 196, 227–241. [Google Scholar] [CrossRef]
  8. Tek, A.; Jiang, J. The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma 2004, 113, 77–83. [Google Scholar] [CrossRef] [PubMed]
  9. Gaspin, C.; Rami, J.F.; Lescure, B. Distribution of short interstitial telomere motifs in two plant genomes: Putative origin and function. BMC Plant Biol. 2010, 10, 1–12. [Google Scholar] [CrossRef]
  10. Mandáková, T.; Gloss, A.D.; Whiteman, N.K.; Lysak, M.A. How diploidization turned a tetraploid into a pseudotriploid. Am. J. Bot. 2016, 103, 1187–1196. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  11. Schwarzacher, T.; Heslop-Harrison, J.S. In situ hybridization to plant telomeres using synthetic oligomers. Genome 1991, 34, 317–323. [Google Scholar] [CrossRef]
  12. Waminal, N.E.; Pellerin, R.J.; Kang, S.H.; Kim, H.H. Chromosomal mapping of tandem repeats revealed massive chromosomal rearrangements and insights into Senna tora dysploidy. Front. Plant Sci. 2021, 12, 154. [Google Scholar] [CrossRef]
  13. Menke, M.; Fuchs, J.; Schubert, I. A comparison of sequence resolution on plant chromosomes: PRINS versus FISH. Theor. Appl. Genet. 1998, 97, 1314–1320. [Google Scholar] [CrossRef]
  14. Jiang, J.; Gill, B.S. Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 2006, 49, 1057–1068. [Google Scholar] [CrossRef] [PubMed]
  15. Figueroa, D.M.; Bass, H.W. A historical and modern perspective on plant cytogenetics. Brief. Funct. Genom. 2010, 9, 95–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Waminal, N.E.; Pellerin, R.J.; Kim, N.S.; Jayakodi, M.; Park, J.Y.; Yang, T.J.; Kim, H.H. Rapid and efficient FISH using pre-labeled oligomer probes. Sci. Rep. 2018, 8, 1–10. [Google Scholar]
  17. Thomas, H.M.; Williams, K.; Harper, J.A. Labelling telomeres of cereals, grasses and clover by primed in situ DNA labelling. Chromosome Res. 1996, 4, 182–184. [Google Scholar] [CrossRef] [PubMed]
  18. Emadzade, K.; Jang, T.S.; Macas, J.; Kovařík, A.; Novák, P.; Parker, J.; Weiss-Schneeweiss, H. Differential amplification of satellite PaB6 in chromosomally hypervariable Prospero autumnale complex (Hyacinthaceae). Ann. Bot. 2014, 114, 1597–1608. [Google Scholar] [CrossRef] [Green Version]
  19. Cuadrado, Á.; Golczyk, H.; Jouve, N. A novel, simple and rapid nondenaturing FISH (ND-FISH) technique for the detection of plant telomeres. Potential used and possible target structures detected. Chromosome Res. 2009, 17, 755–762. [Google Scholar] [CrossRef]
  20. Lou, Q.; Iovene, M.; Spooner, D.M.; Buell, C.R.; Jiang, J. Evolution of chromosome 6 of Solanum species revealed by comparative fluorescence in situ hybridization mapping. Chromosoma 2010, 119, 435–442. [Google Scholar] [CrossRef]
  21. Majerová, E.; Fojtová, M.; Mandáková, T.; Fajkus, J. Methylation of plant telomeric DNA: What do the results say? Plant Mol. Biol. 2011, 77, 533–536. [Google Scholar] [CrossRef]
  22. Majerová, E.; Mandáková, T.; Vu, G.T.; Fajkus, J.; Lysak, M.A.; Fojtová, M. Chromatin features of plant telomeric sequences at terminal vs. internal positions. Front. Plant Sci. 2014, 5, 593. [Google Scholar] [CrossRef] [Green Version]
  23. Sýkorová, E.; Fajkus, J.; Mezníková, M.; Lim, K.Y.; Neplechová, K.; Blattner, F.R.; Leitch, A.R. Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am. J. Bot. 2006, 93, 814–823. [Google Scholar] [CrossRef]
  24. Fajkus, P.; Peška, V.; Sitová, Z.; Fulnečková, J.; Dvořáčková, M.; Gogela, R.; Sýkorová, E.; Fajkus, J. Allium telomeres unmasked: The unusual telomeric sequence (CTCGGTTATGGG)n is synthesized by telomerase. Plant J. 2016, 85, 337–347. [Google Scholar] [CrossRef] [Green Version]
  25. Peška, V.; Fajkus, P.; Fojtová, M.; Dvořáčková, M.; Hapala, J.; Dvořáček, V.; Polanská, P.; Leitch, A.R.; Sýkorová, E.; Fajkus, J. Characterisation of an unusual telomere motif (TTTTTTAGGG)n in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J. 2015, 82, 644–654. [Google Scholar] [CrossRef] [PubMed]
  26. Sýkorová, E.; Lim, K.Y.; Chase, M.W.; Knapp, S.; Leitch, I.J.; Leitch, A.R.; Fajkus, J. The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): First evidence from eudicots. Plant J. 2003, 34, 283–291. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Tran, T.D.; Cao, H.X.; Jovtchev, G.; Neumann, P.; Novák, P.; Fojtová, M.; Vu, G.T.H.; Macas, J.; Fajkus, J.; Schubert, I.; et al. Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea. Plant J. 2015, 84, 1087–1099. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Katsiotis, A.; Hagidimitriou, M.; Heslop-Harrison, J.S. The close relationship between the A and B genomes in Avena L. (Poaceae) determined by molecular cytogenetic analysis of total genomic, tandemly and dispersed repetitive DNA sequences. Ann. Bot. 1997, 79, 103–109. [Google Scholar] [CrossRef] [Green Version]
  29. Hizume, M.; Shibata, F.; Matsusaki, Y.; Kondo, T. Chromosomal localization of telomere sequence repeats in five gymnosperm species. Chromosome Sci. 2000, 4, 39–42. [Google Scholar]
  30. Hizume, M.; Kurose, N.; Shibata, F.; Kondo, K. Molecular cytogenetic studies on sex chromosomes and proximal heterochromatin containing telomere-like sequence in Cycas revoluta. Chromosome Sci. 1998, 2, 63–72. [Google Scholar]
  31. Shibata, F.; Hizume, M. Survey of Arabidopsis-and human-type telomere repeats in plants using fluorescence in situ hybridisation. Cytologia 2011, 76, 353–360. [Google Scholar] [CrossRef] [Green Version]
  32. Hizume, M.; Shibata, F.; Matsusaki, Y.; Garajova, Z. Chromosome identification and comparative karyotypic analyses of four Pinus species. Theor. Appl. Genet. 2002, 105, 491–497. [Google Scholar] [CrossRef]
  33. Shibata, F.; Matsusaki, Y.; Hizume, M. AT-rich sequences containing Arabidopsis-type telomere sequence and their chromosomal distribution in Pinus densiflora. Theor. Appl. Genet. 2005, 110, 1253–1258. [Google Scholar] [CrossRef] [PubMed]
  34. Schmidt, A.; Doudrick, R.L.; Heslop-Harrison, J.S.; Schmidt, T. The contribution of short repeats of low sequence complexity to large conifer genomes. Theor. Appl. Genet. 2000, 101, 7–14. [Google Scholar] [CrossRef]
  35. Islam-Faridi, M.N.; Nelson, C.D.; Kubisiak, T.L. Reference karyotype and cytomolecular map for loblolly pine (Pinus taeda L.). Genome 2007, 50, 241–251. [Google Scholar] [CrossRef] [PubMed]
  36. Murray, B.G.; Friesen, N.; Heslop-Harrison, J.S. Molecular cytogenetic analysis of Podocarpus and comparison with other gymnosperm species. Ann. Bot. 2002, 89, 483–489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Kondo, K.; Tagashira, N. Regions in situ-hybridized by the Arabidopsis-type telomere sequence repeats in Zamia chromosomes. Chromosome Sci. 1998, 2, 87–89. [Google Scholar]
  38. Kondo, K.; Tagashira, N.; Abd El-Twab, M.H.; Hoshi, Y.; Kokubugata, G.; Honda, Y.; Khaung, K.K. Structural differences of chromosomes in plants detected by fluorescence in situ hybridization using probes of rDNA, Arabidopsis-type telomere sequence repeats and pCrT7-4. In Some Aspects of Chromosome Structure and Functions; Sobti, R.C., Obe, G., Athwal, R.S., Eds.; Springer: Dordrecht, The Netherlands, 2002; pp. 27–35. [Google Scholar]
  39. Abd El-Twab, M.H.; Kondo, K. FISH physical mapping of 5S rDNA and telomere sequence repeats identified a peculiar chromosome mapping and mutation in Leucanthemella linearis and Nipponanthemum nipponicum in Chrysanthemum sensu lato. Chromosom. Bot. 2007, 2, 11–17. [Google Scholar] [CrossRef] [Green Version]
  40. Amosova, A.V.; Bolsheva, N.L.; Samatadze, T.E.; Twardovska, M.O.; Zoshchuk, S.A.; Andreev, I.O.; Badaeva, E.D.; Kunakh, V.A.; Muravenko, O.V. Molecular cytogenetic analysis of Deschampsia antarctica Desv. (Poaceae), Maritime Antarctic. PLoS ONE 2015, 10, e0138878. [Google Scholar] [CrossRef]
  41. Begum, R.; Alam, S.S.; Menzel, G.; Schmidt, T. Comparative molecular cytogenetics of major repetitive sequence families of three Dendrobium species (Orchidaceae) from Bangladesh. Ann. Bot. 2009, 104, 863–872. [Google Scholar] [CrossRef] [Green Version]
  42. Begum, R.; Zakrzewski, F.; Menzel, G.; Weber, B.; Alam, S.S.; Schmidt, T. Comparative molecular cytogenetic analyses of a major tandemly repeated DNA family and retrotransposon sequences in cultivated jute Corchorus species (Malvaceae). Ann. Bot. 2013, 112, 123–134. [Google Scholar] [CrossRef] [Green Version]
  43. Bolsheva, N.L.; Zelenin, A.V.; Nosova, I.V.; Amosova, A.V.; Samatadze, T.E.; Yurkevich, O.Y.; Melnikova, N.V.; Zelenina, D.A.; Volkov, A.A.; Muravenko, O.V. The diversity of karyotypes and genomes within section Syllinum of the genus Linum (Linaceae) revealed by molecular cytogenetic markers and RAPD analysis. PLoS ONE 2015, 10, e0122015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Chacón, J.; Sousa, A.; Baeza, C.M.; Renner, S.S. Ribosomal DNA distribution and a genus-wide phylogeny reveal patterns of chromosomal evolution in Alstroemeria (Alstroemeriaceae). Am. J. Bot. 2012, 99, 1501–1512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Navrátilová, A.; Neumann, P.; Macas, J. Karyotype analysis of four Vicia species using in situ hybridization with repetitive sequences. Ann. Bot. 2003, 91, 921–926. [Google Scholar] [CrossRef] [Green Version]
  46. Hanmoto, H.; Kataoka, R.; Ohmido, N.; Yonezawa, Y. Interstitial telomere-like repeats in the Haplopappus gracilis (Asteraceae) genome revealed by fluorescence in situ hybridization. Cytologia 2007, 72, 483–488. [Google Scholar] [CrossRef] [Green Version]
  47. Cuadrado, Á.; Carmona, A.; Jouve, N. Chromosomal characterization of the three subgenomes in the polyploids of Hordeum murinum L.: New insight into the evolution of this complex. PLoS ONE 2013, 8, e81385. [Google Scholar] [CrossRef] [Green Version]
  48. Da Silva, C.R.; González-Elizondo, M.S.; Vanzela, A.L. Reduction of chromosome number in Eleocharis subarticulata (Cyperaceae) by multiple translocations. Bot. J. Linn. Soc. 2005, 149, 457–464. [Google Scholar] [CrossRef]
  49. Deng, H.; Tang, G.; Xu, N.; Gao, Z.; Lin, L.; Liang, D.; Xia, H.; Deng, Q.; Wang, J.; Cai, Z.; et al. Integrated karyotypes of diploid and tetraploid Carrizo Citrange (Citrus sinensis L. Osbeck × Poncirus trifoliata L. Raf.) as determined by sequential multicolor fluorescence in situ hybridization with tandemly repeated DNA sequences. Front Plant Sci. 2020, 11, 569. [Google Scholar] [CrossRef]
  50. Du, P.; Li, L.N.; Zhang, Z.X.; Liu, H.; Qin, L.; Huang, B.Y.; Dong, W.; Tang, F.; Qi, Z.; Zhang, X.Y. Chromosome painting of telomeric repeats reveals new evidence for genome evolution in peanut. J. Integr. Agric. 2016, 15, 2488–2496. [Google Scholar] [CrossRef] [Green Version]
  51. Zhang, L.; Yang, X.; Tia, L.; Chen, L.; Yu, W. Identification of peanut (Arachis hypogaea) chromosomes using a fluorescence in situ hybridization system reveals multiple hybridization events during tetraploid peanut formation. New Phytol. 2016, 211, 1424–1439. [Google Scholar] [CrossRef]
  52. Falistocco, E. Insight into the chromosome structure of the cultivated tetraploid alfalfa (Medicago sativa subsp. sativa L.) by a combined use of GISH and FISH techniques. Plants 2020, 9, 542. [Google Scholar] [CrossRef] [PubMed]
  53. Dechyeva, D.; Schmidt, T. Molecular organization of terminal repetitive DNA in Beta species. Chromosome Res. 2006, 14, 881–897. [Google Scholar] [CrossRef]
  54. Zatloukalová, P.; Hřibová, E.; Kubaláková, M.; Suchánková, P.; Šimková, H.; Adoración, C.; Kahl, G.; Millán, T.; Doležel, J. Integration of genetic and physical maps of the chickpea (Cicer arietinum L.) genome using flow-sorted chromosomes. Chromosome Res. 2011, 19, 729–739. [Google Scholar] [CrossRef]
  55. Gortner, G.; Nenno, M.; Weising, K.; Zink, D.; Nagl, W.; Kahl, G. Chromosomal localization and distribution of simple sequence repeats and the Arabidopsis-type telomere sequence in the genome of Cicer arietinum L. Chromosome Res. 1998, 6, 97–104. [Google Scholar] [CrossRef] [PubMed]
  56. Grabowska-Joachimiak, A.; Mosiolek, M.; Lech, A.; Góralski, G. C-Banding/DAPI and in situ hybridization reflect karyotype structure and sex chromosome differentiation in Humulus japonicus Siebold & Zucc. Cytogenet. Genome Res. 2011, 132, 203–211. [Google Scholar] [PubMed]
  57. Grabowska-Joachimiak, A.; Kula, A.; Gernand-Kliefoth, D.; Joachimiak, A.J. Karyotype structure and chromosome fragility in the grass Phleum echinatum Host. Protoplasma 2015, 252, 301–306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. He, L.; Liu, J.; Torres, G.A.; Zhang, H.; Jiang, J.; Xie, C. Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosome Res. 2013, 21, 5–13. [Google Scholar] [CrossRef] [PubMed]
  59. Zhang, Y.; Cheng, C.; Li, J.; Yang, S.; Wang, Y.; Li, Z.; Chen, J.; Lou, Q. Chromosomal structures and repetitive sequences divergence in Cucumis species revealed by comparative cytogenetic mapping. BMC Genom. 2015, 16, 1–13. [Google Scholar] [CrossRef] [Green Version]
  60. Koo, D.H.; Hong, C.P.; Batley, J.; Chung, Y.S.; Edwards, D.; Bang, J.W.; Hur, Y.; Lim, Y.P. Rapid divergence of repetitive DNAs in Brassica relatives. Genomics 2011, 97, 173–185. [Google Scholar] [CrossRef] [Green Version]
  61. Kim, E.S.; Bolshev, N.L.; Samatadze, T.E.; Nosov, N.N.; Nosova, I.V.; Zelenin, A.V.; Punina, E.O.; Muravenko, O.V.; Rodionov, A.V. The unique genome of two-chromosome grasses Zingeria and Colpodium, its origin, and evolution. Russ. J. Genet. 2009, 45, 1329–1337. [Google Scholar] [CrossRef]
  62. Kirov, I.V.; Van Laere, K.; Van Roy, N.; Khrustaleva, L.I. Towards a FISH-based karyotype of Rosa L. (Rosaceae). Comp. Cytogenet. 2016, 10, 543. [Google Scholar] [CrossRef] [PubMed]
  63. Kondo, K.; Furuta, T. Region in situ-hybridized by the Arabidopsis-type telomere sequence repeats in Drosera chromosomes. Chromosome Sci. 1999, 3, 63–67. [Google Scholar]
  64. Kono, Y.; Hoshi, Y.; Setoguchi, H.; Yokota, M.; Oginuma, K. Distribution patterns rDNAs and telomeres and chromosomal rearrangement between two cytotypes of Lysimachia mauritiana L. (Primulaceae). Caryologia 2011, 64, 91–98. [Google Scholar] [CrossRef]
  65. Kono, Y.; Peng, C.I.; Hoshi, Y.; Yokota, M.; Setoguchi, H.; Lum, S.K.; Oginuma, K. Intraspecific karyotype polymorphism and chromosomal evolution of Lysimachia mauritiana (Primulaceae) in the Ryukyu archipelago of Japan and Taiwan. Cytologia 2019, 84, 93–103. [Google Scholar] [CrossRef]
  66. Lan, T.Y.; Liu, B.; Dong, F.P.; Chen, R.Y.; Li, X.L.; Chen, C.B. Multicolor FISH analysis of rDNA and telomere on spinach. Front Agric. China 2008, 29, 1405–1408. [Google Scholar] [CrossRef]
  67. Li, J.; He, S.; Zhang, L.; Hu, Y.; Yang, F.; Ma, L.; Huang, J.; Li, L. Telomere and 45S rDNA sequences are structurally linked on the chromosomes in Chrysanthemum segetum L. Protoplasma 2012, 249, 207–215. [Google Scholar] [CrossRef]
  68. Luo, X.; Chen, J. Physical map of FISH 5S rDNA and (AG3T3)3 signals displays Chimonanthus campanulatus R.H. Chang & C.S. Ding chromosomes, reproduces its metaphase dynamics and distinguishes its chromosomes. Genes 2019, 10, 904. [Google Scholar]
  69. Maravilla, A.J.; Rosato, M.; Álvarez, I.; Nieto Feliner, G.; Rosselló, J.A. Interstitial Arabidopsis-type telomeric repeats in Asteraceae. Plants 2021, submitted. [Google Scholar]
  70. Mlinarec, J.; Skuhala, A.; Jurković, A.; Malenica, N.; McCann, J.; Weiss-Schneeweiss, H.; Bohanec, B.; Besendorfer, V. The repetitive DNA composition in the natural pesticide producer Tanacetum cinerariifolium: Interindividual variation of subtelomeric tandem repeats. Front. Plant Sci. 2019, 10, 613. [Google Scholar] [CrossRef]
  71. Moscone, E.A.; Samuel, R.; Schwarzacher, T.; Schweizer, D.; Pedrosa-Harand, A. Complex rearrangements are involved in Cephalanthera (Orchidaceae) chromosome evolution. Chromosome Res. 2007, 15, 931–943. [Google Scholar] [CrossRef]
  72. Németh, A.V.; Dudits, D.; Molnár-Láng, M.; Linc, G. Molecular cytogenetic characterisation of Salix viminalis L. using repetitive DNA sequences. J. Appl. Genet. 2013, 54, 265–269. [Google Scholar] [CrossRef] [Green Version]
  73. Nenno, M.; Zink, D.; Nagl, W. The Arabidopsis telomere sequence is highly abundant in the genome of Phaseolus acutifolius and preferentially located in the centromeres. Rep. Bean Improv. Coop. Nat. Dry Bean Counc. Res. Conf. Ann. Rep. 1998, 41, 103–104. [Google Scholar]
  74. Nguyen, T.H.; Waminal, N.E.; Lee, D.S.; Pellerin, R.J.; Ta, T.D.; Campomayor, N.B.; Kang, B.Y.; Kim, H.H. Comparative triple-color FISH mapping in eleven Senna species using rDNA and telomeric repeat probes. Hortic. Environ. Biotechnol. 2021, 62, 927–935. [Google Scholar] [CrossRef]
  75. Pedrosa, A.; Sandal, N.; Stougaard, J.; Schweizer, D.; Bachmair, A. Chromosomal map of the model legume Lotus japonicus. Genetics 2002, 161, 1661–1672. [Google Scholar] [CrossRef]
  76. Pellerin, R.J.; Waminal, N.E.; Kim, H.H. Triple-color FISH karyotype analysis of four Korean wild Cucurbitaceae species. Hortic. Sci. Technol. 2018, 36, 98–107. [Google Scholar]
  77. Pellerin, R.J.; Waminal, N.E.; Kim, H.H. FISH mapping of rDNA and telomeric repeats in 10 Senna species. Hortic. Environ. Biotechnol. 2019, 60, 253–260. [Google Scholar] [CrossRef]
  78. Raskina, O.; Barber, J.C.; Nevo, E.; Belyayev, A. Repetitive DNA and chromosomal rearrangements: Speciation-related events in plant genomes. Cytogenet. Genome Res. 2008, 120, 351–357. [Google Scholar] [CrossRef]
  79. Uchida, W.; Matsunaga, S.; Sugiyama, R.; Kawano, S. Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes Genet. Syst. 2002, 77, 63–67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  80. Uchida, W.; Matsunaga, S.; Sugiyama, R.; Shibata, F.; Kazama, Y.; Miyazawa, Y.; Hizume, M.; Kawano, S. Distribution of interstitial telomere-like repeats and their adjacent sequences in a dioecious plant, Silene latifolia. Chromosoma 2002, 111, 313–320. [Google Scholar] [CrossRef] [PubMed]
  81. Rockinger, A.; Sousa, A.; Carvalho, F.A.; Renner, S.S. Chromosome number reduction in the sister clade of Carica papaya with concomitant genome size doubling. Am. J. Bot. 2016, 103, 1082–1088. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Rosato, M.; Álvarez, I.; Nieto Feliner, G.; Rosselló, J.A. Inter-and intraspecific hypervariability in interstitial telomeric-like repeats (TTTAGGG)n in Anacyclus (Asteraceae). Ann. Bot. 2018, 122, 387–395. [Google Scholar] [CrossRef]
  83. Sevilleno, S.S.; Ju, Y.H.; Kim, J.S.; Mancia, F.H.; Byeon, E.J.; Cabahug, R.A.; Hwang, Y.J. Cytogenetic analysis of Bienertia sinuspersici Akhani as the first step in genome sequencing. Genes Genom. 2020, 42, 337–345. [Google Scholar] [CrossRef]
  84. Sousa, A.; Renner, S.S. Interstitial telomere-like repeats in the monocot family Araceae. Bot. J. Linn. Soc. 2015, 177, 15–26. [Google Scholar] [CrossRef] [Green Version]
  85. Sousa, A.; Cusimano, N.; Renner, S.S. Combining FISH and model-based predictions to understand chromosome evolution in Typhonium (Araceae). Ann. Bot. 2014, 113, 669–680. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Souza, G.; Vanzela, A.L.; Crosa, O.; Guerra, M. Interstitial telomeric sites and Robertsonian translocations in species of Ipheion and Nothoscordum (Amaryllidaceae). Genetica 2016, 144, 157–166. [Google Scholar] [CrossRef] [PubMed]
  87. Sýkorová, E.; Lim, K.Y.; Fajkus, J.; Leitch, A.R. The signature of the Cestrum genome suggests an evolutionary response to the loss of (TTTAGGG)n telomeres. Chromosoma 2003, 112, 164–172. [Google Scholar] [CrossRef] [PubMed]
  88. Vasconcelos, E.V.; Vasconcelos, S.; Ribeiro, T.; Benko-Iseppon, A.M.; Brasileiro-Vidal, A.C. Karyotype heterogeneity in Philodendron s.l. (Araceae) revealed by chromosome mapping of rDNA loci. PLoS ONE 2018, 13, e0207318. [Google Scholar] [CrossRef]
  89. Waminal, N.E.; Pellerin, R.J.; Jang, W.; Kim, H.H.; Yang, T.J. Characterization of chromosome-specific microsatellite repeats and telomere repeats based on low coverage whole genome sequence reads in Panax ginseng. Plant Breed. Biotechnol. 2018, 6, 74–81. [Google Scholar] [CrossRef]
  90. Waminal, N.E.; Yang, T.J.; In, J.G.; Kim, H.H. Five-color fluorescence in situ hybridization system for karyotyping of Panax ginseng. Hortic. Environ. Biotechnol. 2020, 61, 869–877. [Google Scholar] [CrossRef]
  91. Weiss-Schneeweiss, H.; Riha, K.; Jang, C.G.; Puizina, J.; Scherthan, H.; Schweizer, D. Chromosome termini of the monocot plant Othocallis siberica are maintained by telomerase, which specifically synthesises vertebrate-type telomere sequences. Plant J. 2004, 37, 484–493. [Google Scholar] [CrossRef]
  92. Deng, H.; Xiang, S.; Guo, Q.; Jin, W.; Cai, Z.; Liang, G. Molecular cytogenetic analysis of genome-specific repetitive elements in Citrus clementina Hort. ex Tan. and its taxonomic implications. BMC Plant Biol. 2019, 19, 77. [Google Scholar] [CrossRef]
  93. Deng, H.; Cai, Z.; Xiang, S.; Guo, Q.; Huang, W.; Liang, G. Karyotype analysis of diploid and spontaneously occurring tetraploid blood orange [Citrus sinensis (L.) Osbeck] using multicolor FISH with repetitive DNA sequences as probes. Front. Plant Sci. 2019, 10, 331. [Google Scholar] [CrossRef]
  94. Prieto, P.; Martín, A.; Cabrera, A. Chromosomal distribution of telomeric and telomeric-associated sequences in Hordeum chilense by in situ hybridization. Hereditas 2004, 141, 122–127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Castiglione, M.R.; Kotseruba, V.; Cremonini, R. Methylated-rich regions and tandem repeat arrays along the chromosome complement of Colpodium versicolor (Stev.) Schmalh. Protoplasma 2009, 237, 13. [Google Scholar] [CrossRef]
  96. Heckmann, S.; Schroeder-Reiter, E.; Kumke, K.; Ma, L.; Nagaki, K.; Murata, M.; Wanner, G.; Houben, A. Holocentric chromosomes of Luzula elegans are characterized by a longitudinal centromere groove, chromosome bending, and a terminal nucleolus organizer region. Cytogenet. Genome Res. 2011, 134, 220–228. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Maximiano Da Silva, C.M.; González-Elizondo, M.S.; Laforga Vanzela, A.L. Chromosome reduction in Eleocharis maculosa (Cyperaceae). Cytogenet Genome Res. 2008, 122, 175–180. [Google Scholar] [CrossRef] [PubMed]
  98. Hoshi, Y.; Yagi, K.; Matsuda, M.; Matoba, H.; Tagashira, N.; Pląder, W.; Malepszy, S.; Nagano, K.; Morikawa, A. A comparative study of the three cucumber cultivars using fluorescent staining and fluorescence in situ hybridization. Cytologia 2011, 76, 3–10. [Google Scholar] [CrossRef] [Green Version]
  99. Pellerin, R.J.; Waminal, N.E.; Belandres, H.R.; Kim, H.H. Karyotypes of three exotic cucurbit species based on triple-color FISH analysis. Korean J. Hortic. Sci. Technol. 2018, 36, 417–425. [Google Scholar]
  100. Alexandrov, O.S.; Divashuk, M.G.; Yakovin, N.A.; Karlov, G.I. Sex chromosome differentiation in Humulus japonicus Siebold & Zuccarini, 1846 (Cannabaceae) revealed by fluorescence in situ hybridization of subtelomeric repeat. Comp. Cytogenet. 2012, 6, 239. [Google Scholar]
  101. Divashuk, M.G.; Alexandrov, O.S.; Kroupin, P.Y.; Karlov, G.I. Molecular cytogenetic mapping of Humulus lupulus sex chromosomes. Cytogenet Genome Res. 2011, 134, 213–219. [Google Scholar] [CrossRef] [PubMed]
  102. Hasterok, R.; Ksiazczyk, T.; Wolny, E.; Maluszynska, J. FISH and GISH analysis of Brassica genomes. Acta Biol. Cracov. Bot. 2005, 47, 185–192. [Google Scholar]
  103. Adams, S.P.; Hartman, T.P.V.; Lim, K.Y.; Chase, M.W.; Bennett, M.D.; Leitch, I.J.; Leitch, A.R. Loss and recovery of Arabidopsis–type telomere repeat sequences 5′–(TTTAGGG)n–3′ in the evolution of a major radiation of flowering plants. Proc. R. Soc. Lond. B. Biol. Sci. 2001, 268, 1541–1546. [Google Scholar] [CrossRef] [Green Version]
  104. Jacobs, G.; Dechyeva, D.; Wenke, T.; Weber, B.; Schmidt, T. A BAC library of Beta vulgaris L. for the targeted isolation of centromeric DNA and molecular cytogenetics of Beta species. Genetica 2009, 135, 157–167. [Google Scholar] [CrossRef]
  105. Puizina, J.; Sviben, T.; Krajačić-Sokol, I.; Zoldoš-Pećnik, V.; Siljak-Yakovlev, S.; Papeš, D.; Besendorfer, V. Cytogenetic and molecular characterization of the Abies alba genome and its relationship with other members of the Pinaceae. Plant Biol. 2008, 10, 256–267. [Google Scholar] [CrossRef]
  106. Lubaretz, O.; Fuch, J.; Ahne, R.; Meister, A.; Schubert, I. Karyotyping of three Pinaceae species via fluorescent in situ hybridization and computer-aided chromosome analysis. Theor. Appl. Genet. 1996, 92, 411–416. [Google Scholar] [CrossRef]
  107. de la Herrán, R.; Cuñado, N.; Navajas-Pérez, R.; Santos, J.L.; Rejón, C.R.; Garrido-Ramos, M.A.; Rejón, M.R. The controversial telomeres of lily plants. Cytogenet. Genome Res. 2005, 109, 144–147. [Google Scholar] [CrossRef] [PubMed]
  108. Sýkorová, E.; Lim, K.Y.; Kunická, Z.; Chase, M.W.; Bennett, M.D.; Fajkus, J.; Leitch, A.R. Telomere variability in the monocotyledonous plant order Asparagales. Proc. R. Soc. Lond. B Biol. Sci. 2003, 270, 1893–1904. [Google Scholar] [CrossRef]
  109. Monkheang, P.; Chaveerach, A.; Sudmoon, R.; Tanee, T. Karyotypic features including organizations of the 5S, 45S rDNA loci and telomeres of Scadoxus multiflorus (Amaryllidaceae). Comp. Cytogenet. 2016, 10, 637. [Google Scholar]
  110. Báez, M.; Souza, G.; Guerra, M. Genome size and cytomolecular diversification in two species of the South African endemic genus Tulbaghia L. (Allioideae, Amaryllidaceae). S. Afr. J. Bot. 2020, 130, 407–413. [Google Scholar] [CrossRef]
  111. Falistocco, E.; Ferradini, N. Advances in the cytogenetics of Annonaceae, the case of Annona cherimola L. Genome 2020, 63, 357–364. [Google Scholar] [CrossRef]
  112. Nowicka, A.; Grzebelus, E.; Grzebelus, D. Precise karyotyping of carrot mitotic chromosomes using multicolour-FISH with repetitive DNA. Biol. Plant. 2016, 60, 25–36. [Google Scholar] [CrossRef]
  113. Zhou, H.C.; Pellerin, R.J.; Waminal, N.E.; Yang, T.J.; Kim, H.H. Pre-labelled oligo probe-FISH karyotype analyses of four Araliaceae species using rDNA and telomeric repeat. Genes Genom. 2019, 41, 839–847. [Google Scholar] [CrossRef] [PubMed]
  114. Castilho, A.; Vershinin, A.; Heslop-Harrison, J.S. Repetitive DNA and the chromosomes in the genome of oil palm (Elaeis guineensis). Ann. Bot. 2000, 85, 837–844. [Google Scholar] [CrossRef] [Green Version]
  115. Zaki, N.M. The genome landscape of Elaeis guineensis: Development and Utility of Chromosome-Specific Cytogenetic Markers. Ph.D. Thesis, University of Leicester, Leicester, UK, April 2019. [Google Scholar]
  116. Pereira, T.N.S.; Neto, M.F.; de Souza, M.M.; da Costa Geronimo, I.G.; de Melo, C.A.F.; Pereira, M.G. Cytological characterization of Brazilian green dwarf coconut (Cocos nucifera L.) via meiosis and conventional and differential karyotyping. Cytologia 2017, 82, 167–174. [Google Scholar] [CrossRef]
  117. Robert, M.L.; Lim, K.Y.; Hanson, L.; Sanchez-Teyer, F.; Bennett, M.D.; Leitch, A.R.; Leitch, I.J. Wild and agronomically important Agave species (Asparagaceae) show proportional increases in chromosome number, genome size, and genetic markers with increasing ploidy. Bot. J. Linn. Soc. 2008, 158, 215–222. [Google Scholar] [CrossRef] [Green Version]
  118. Puizina, J.; Weiss-Schneeweiss, H.; Pedrosa-Harand, A.; Kamenjarin, J.; Trinajstić, I.; Riha, K.; Schweizer, D. Karyotype analysis in Hyacinthella dalmatica (Hyacinthaceae) reveals vertebrate-type telomere repeats at the chromosome ends. Genome 2003, 46, 1070–1076. [Google Scholar] [CrossRef]
  119. Weiss, H.; Scherthan, H. Aloe spp.–plants with vertebrate-like telomeric sequences. Chromosome Res. 2002, 10, 155–164. [Google Scholar] [CrossRef] [PubMed]
  120. Abd El-Twab, M.H.; Kondo, K. Physical mapping of 5S, 45S, Arabidopsis-type telomere sequence repeats and AT-rich regions in Achillea millefolium showing intrachromosomal variation by FISH and DAPI. Chromosom. Bot. 2009, 4, 37–45. [Google Scholar] [CrossRef]
  121. Borgen, L.; Leitch, I.; Santos-Guerra, A. Genome organization in diploid hybrid species of Argyranthemum (Asteraceae) in the Canary Islands. Bot. J. Linn. Soc. 2003, 141, 491–501. [Google Scholar] [CrossRef]
  122. García, S.; Garnatje, T.; Pellicer, J.; McArthur, E.D.; Siljak-Yakovlev, S.; Vallés, J. Ribosomal DNA, heterochromatin, and correlation with genome size in diploid and polyploid North American endemic sagebrushes (Artemisia, Asteraceae). Genome 2009, 52, 1012–1024. [Google Scholar] [CrossRef] [Green Version]
  123. Matoba, H.; Uchiyama, H. Physical mapping of 5S rDNA, 18S rDNA and telomere sequences in three species of the genus Artemisia (Asteraceae) with distinct basic chromosome numbers. Cytologia 2009, 74, 115–123. [Google Scholar] [CrossRef] [Green Version]
  124. Houben, A.; Thompson, N.; Ahne, R.; Leach, C.R.; Verlin, D.; Timmis, J.N. A monophyletic origin of the B chromosomes of Brachycome dichromosomatica (Asteraceae). Plant Syst. Evol. 1999, 219, 127–135. [Google Scholar] [CrossRef]
  125. Mancia, F.H.; Ju, Y.H.; Lim, K.B.; Kim, J.S.; Nam, S.Y.; Hwang, Y.J. Cytogenetic mapping of Carthamus tinctorius L. with tandemly repeated DNA sequences by fluorescence in situ hybridization. Korean J. Plant Res. 2017, 30, 654–661. [Google Scholar]
  126. Dydak, M.; Kolano, B.; Nowak, T.; Siwinska, D.; Maluszynska, J. Cytogenetic studies of three European species of Centaurea L. (Asteraceae). Hereditas 2009, 146, 152–161. [Google Scholar] [CrossRef] [PubMed]
  127. Cuyacot, A.R.; Won, S.Y.; Park, S.K.; Sohn, S.H.; Lee, J.; Kim, J.S.; Kim, H.H.; Lim, K.M.; Hwang, Y.J. The chromosomal distribution of repetitive DNA sequences in Chrysanthemum boreale revealed a characterization in its genome. Sci. Hortic. 2016, 198, 438–444. [Google Scholar] [CrossRef]
  128. Abd El-Twab, M.H.; Kondo, K. FISH physical mapping of 5S, 45S and Arabidopsis-type telomere sequence repeats in Chrysanthemum zawadskii showing intra-chromosomal variation and complexity in nature. Chromosom. Bot. 2006, 1, 1–5. [Google Scholar] [CrossRef] [Green Version]
  129. Cuyacot, A.R.; Lim, K.B.; Kim, H.H.; Hwang, Y.J. Chromosomal characterization based on repetitive DNA distribution in a tetraploid cytotype of Chrysanthemum zawadskii. Hortic. Environ. Biotechnol 2017, 58, 488–494. [Google Scholar] [CrossRef]
  130. Jamilena, M.; Rejón, C.R.; Rejón, M.R. A molecular analysis of the origin of the Crepis capillaris B chromosome. J. Cell Sci. 1994, 107, 703–708. [Google Scholar] [CrossRef] [PubMed]
  131. Matoba, H.; Mizutani, T.; Nagano, K.; Hoshi, Y.; Uchiyama, H. Chromosomal study of lettuce and its allied species (Lactuca spp.; Asteraceae) by means of karyotype analysis and fluorescence in situ hybridization. Hereditas 2007, 144, 235–243. [Google Scholar] [CrossRef]
  132. Pires, J.C.; Lim, K.Y.; Kovarík, A.; Matyásek, R.; Boyd, A.; Leitch, A.R.; Bennett, N.D.; Soltis, P.S.; Soltis, D.E. Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors. Am. J. Bot. 2004, 91, 1022–1035. [Google Scholar] [CrossRef] [Green Version]
  133. Liu, J.; Luo, X. First report of bicolour FISH of Berberis diaphana and B. soulieana reveals interspecific differences and co-localization of (AGGGTTT)3 and rDNA 5S in B. diaphana. Hereditas 2019, 156, 1–8. [Google Scholar] [CrossRef]
  134. Mandáková, T.; Marhold, K.; Lysak, M.A. The widespread crucifer species Cardamine flexuosa is an allotetraploid with a conserved subgenomic structure. New Phytol. 2014, 201, 982–992. [Google Scholar] [CrossRef] [PubMed]
  135. Mandáková, T.; Heenan, P.B.; Lysak, M.A. Island species radiation and karyotypic stasis in Pachycladon allopolyploids. BMC Evol. Biol. 2010, 10, 367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  136. Pellerin, R.J.; Waminal, N.E.; Kim, J.Y.; Um, Y.; Kim, H.H. Fluorescence in situ hybridization karyotype analysis of seven Platycodon grandiflorum (Jacq.) A. DC. cultivars. Korean. J. Hortic. Sci. Technol. 2017, 35, 784–792. [Google Scholar]
  137. Vanzela, A.L.L.; Cuadrado, Á.; Vieira, A.O.S.; Jouve, N. Genome characterization and relationships between two species of the genus Lobelia (Campanulaceae) determined by repeated DNA sequences. Plant Syst. Evol. 1999, 214, 211–218. [Google Scholar] [CrossRef]
  138. Divashuk, M.G.; Alexandrov, O.S.; Razumova, O.V.; Kirov, I.V.; Karlov, G.I. Molecular cytogenetic characterization of the dioecious Cannabis sativa with an XY chromosome sex determination system. PLoS ONE 2014, 9, e85118. [Google Scholar]
  139. Iovene, M.; Yu, Q.; Ming, R.; Jiang, J. Evidence for emergence of sex-determining gene(s) in a centromeric region in Vasconcellea parviflora. Genetics 2015, 199, 413–421. [Google Scholar] [CrossRef] [Green Version]
  140. Riha, K.; Fajkus, J.; Siroky, J.; Vyskot, B. Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 1998, 10, 1691–1698. [Google Scholar] [CrossRef] [Green Version]
  141. Sousa, A.; Fuchs, J.; Renner, S.S. Cytogenetic comparison of heteromorphic and homomorphic sex chromosomes in Coccinia (Cucurbitaceae) points to sex chromosome turnover. Chromosome Res. 2017, 25, 191–200. [Google Scholar] [CrossRef]
  142. Vanzela, A.L.; Cuadrado, A.; Guerra, M. Localization of 45S rDNA and telomeric sites on holocentric chromosomes of Rhynchospora tenuis Link (Cyperaceae). Genet. Mol. Biol. 2003, 26, 199–201. [Google Scholar] [CrossRef] [Green Version]
  143. Leitch, A.R.; Lim, K.Y.; Leitch, I.J.; O’Neill, M.; Chye, M.; Low, F. Molecular cytogenetic studies in rubber, Hevea brasiliensis Muell. Arg. (Euphorbiaceae). Genome 1998, 41, 464–467. [Google Scholar] [CrossRef] [Green Version]
  144. Galasso, I.; Schmidt, T.; Pignone, D. Identification of Lens culinaris ssp. culinaris chromosomes by physical mapping of repetitive DNA sequences. Chromosome Res. 2001, 9, 199–209. [Google Scholar] [CrossRef]
  145. Hajdera, I.; Siwinska, D.; Hasterok, R.; Maluszynska, J. Molecular cytogenetic analysis of genome structure in Lupinus angustifolius and Lupinus cosentinii. Theor. Appl. Genet. 2003, 107, 988–996. [Google Scholar] [CrossRef]
  146. Kaczmarek, A.; Naganowska, B.; Wolko, B. Karyotyping of the narrow-leafed lupin (Lupinus angustifolius L.) by using FISH, PRINS and computer measurements of chromosomes. J. Appl. Genet. 2009, 50, 77–82. [Google Scholar] [CrossRef] [PubMed]
  147. Fonsêca, A.; Ferraz, M.E.; Pedrosa-Harand, A. Speeding up chromosome evolution in Phaseolus: Multiple rearrangements associated with a one-step descending dysploidy. Chromosoma 2016, 125, 413–421. [Google Scholar] [CrossRef]
  148. Rawlins, D.J.; Highett, M.I.; Shaw, P.J. Localization of telomeres in plant interphase nuclei by in situ hybridization and 3D confocal microscopy. Chromosoma 1991, 100, 424–431. [Google Scholar] [CrossRef]
  149. Macas, J.; Neumann, P.; Navrátilová, A. Repetitive DNA in the pea (Pisum sativum L.) genome: Comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genom. 2007, 8, 1–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  150. Youn, S.M.; Kim, H.H. Chromosome karyotyping of Senna covesii and S. floribunda based on triple–color FISH mapping of rDNAs and telomeric repeats. Plant Breed. Biotechnol. 2018, 6, 51–56. [Google Scholar] [CrossRef] [Green Version]
  151. Galasso, I.; Schmidt, T.; Pignone, D.; Heslop-Harrison, J.S. The molecular cytogenetics of Vigna unguiculata (L.) Walp: The physical organization and characterization of 18S-5.8S-25S rRNA genes, 5S rRNA genes, telomere-like sequences, and a family of centromeric repetitive DNA sequences. Theor. Appl. Genet. 1995, 91, 928–935. [Google Scholar] [CrossRef]
  152. Jankowska, M.; Fuchs, J.; Klocke, E.; Fojtová, M.; Polanská, P.; Fajkus, J.; Schubert, V.; Houben, A. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma 2015, 124, 519–528. [Google Scholar] [CrossRef]
  153. Xie, S.; Marasek-Ciolakowska, A.; Ramanna, M.S.; Arens, P.; Visser, R.G.; van Tuyl, J.M. Characterization of B chromosomes in Lilium hybrids through GISH and FISH. Plant Syst. Evol. 2014, 300, 1771–1777. [Google Scholar] [CrossRef]
  154. Lombello, R.A.; Forni-Martins, E.R. Cytogenetics and evolutionary analysis of Lophanthera, an Amazonian arboreal Malpighiaceae. Cytologia 2002, 67, 41–45. [Google Scholar] [CrossRef] [Green Version]
  155. Islam-Faridi, N.; Sakhanokho, H.F.; Nelson, C.D. New chromosome number and cyto-molecular characterization of the African Baobab (Adansonia digitata L.)—“The Tree of Life”. Sci. Rep. 2020, 10, 1–15. [Google Scholar] [CrossRef]
  156. Ling, J.; Cheng, H.; Liu, F.; Song, G.L.; Wang, C.Y.; Li, S.H.; Zhang, X.D.; Wang, Y.H.; Wang, K.B. The cloning and fluorescence in situ hybridization analysis of cotton telomere sequence. J. Integr. Agric. 2012, 11, 1417–1423. [Google Scholar] [CrossRef]
  157. Osuji, J.O.; Crouch, J.; Harrison, G.; Heslop-Harrison, J.S. Molecular cytogenetics of Musa species, cultivars and hybrids: Location of 18S-5.8 S-25S and 5S rDNA and telomere-like sequences. Ann. Bot. 1998, 82, 243–248. [Google Scholar] [CrossRef] [Green Version]
  158. Luo, X.; Liu, J. Fluorescence in situ hybridization (FISH) analysis of the locations of the oligonucleotides 5S rDNA, (AGGGTTT)3, and (TTG)6 in three genera of Oleaceae and their phylogenetic framework. Genes 2019, 10, 375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  159. Golczyk, H.; Massouh, A.; Greiner, S. Translocations of chromosome end-segments and facultative heterochromatin promote meiotic ring formation in evening primroses. Plant Cell 2014, 26, 1280–1293. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  160. Zhou, H.C.; Park, E.J.; Kim, H.H. Analysis of chromosome composition of Gastrodia elata Blume by fluorescent in situ hybridization using rDNA and telomeric repeat probes. Korean J. Med. Crop Sci. 2018, 26, 113–118. [Google Scholar] [CrossRef]
  161. de Melo, C.A.F.; Souza, M.M.; Silva, G.S. Karyotype analysis by FISH and GISH techniques on artificial backcrossed interspecific hybrids involving Passiflora sublanceolata (Killip) MacDougal (Passifloraceae). Euphytica 2017, 213, 161. [Google Scholar] [CrossRef]
  162. Dhar, M.K.; Kaul, S.; Friebe, B.; Gill, B.S. Chromosome identification in Plantago ovata Forsk. through C-banding and FISH. Curr. Sci. 2002, 83, 150–152. [Google Scholar]
  163. Shams, I.; Raskina, O. Supernumerary B chromosomes and plant genome changes: A snapshot of wild populations of Aegilops speltoides Tausch (Poaceae, Triticeae). Int. J. Mol. Sci. 2020, 21, 3768. [Google Scholar] [CrossRef]
  164. Santos, F.C.; Guyot, R.; do Valle, C.B.; Chiari, L.; Techio, V.H.; Heslop-Harrison, P.; Vanzela, A.L.L. Chromosomal distribution and evolution of abundant retrotransposons in plants: Gypsy elements in diploid and polyploid Brachiaria forage grasses. Chromosome Res. 2015, 23, 571–582. [Google Scholar] [CrossRef] [Green Version]
  165. Rocha, L.C.; de Oliveira Bustamante, F.; Silveira, R.A.D.; Torres, G.A.; Mittelmann, A.; Techio, V.H. Functional repetitive sequences and fragile sites in chromosomes of Lolium perenne L. Protoplasma 2015, 252, 451–460. [Google Scholar] [CrossRef]
  166. Jiang, J.; Gill, B.S.; Wang, G.L.; Ronald, P.C.; Ward, D.C. Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc. Natl. Acad. Sci. USA 1995, 92, 4487–4491. [Google Scholar] [CrossRef] [Green Version]
  167. Cheng, Z.; Stupar, R.M.; Gu, M.; Jiang, J. A tandemly repeated DNA sequence is associated with both knob-like heterochromatin and a highly decondensed structure in the meiotic pachytene chromosomes of rice. Chromosoma 2001, 110, 24–31. [Google Scholar] [CrossRef]
  168. Manzanero, S.; Puertas, M.J. Rye terminal neocentromeres: Characterisation of the underlying DNA and chromatin structure. Chromosoma 2003, 111, 408–415. [Google Scholar] [CrossRef] [PubMed]
  169. Werner, J.E.; Kota, R.S.; Gill, B.S.; Endo, T.R. Distribution of telomeric repeats and their role in the healing of broken chromosome ends in wheat. Genome 1992, 35, 844–848. [Google Scholar] [CrossRef]
  170. Mlinarec, J.; Papeš, D.A.; Besendorfer, V. Ribosomal, telomeric and heterochromatin sequences localization in the karyotype of Anemone hortensis. Bot. J. Linn. Soc. 2006, 150, 177–186. [Google Scholar] [CrossRef] [Green Version]
  171. Schuster, M.; Fuchs, J.; Schubert, I. Cytogenetics in fruit breeding-localization of ribosomal RNA genes on chromosomes of apple (Malus × domestica Borkh.). Theor. Appl. Genet. 1997, 94, 322–324. [Google Scholar] [CrossRef]
  172. Yu, C.; Deng, X.; Chen, C. Chromosomal characterization of a potential model mini-Citrus (Fortunella hindsii). Tree Genet. Genomes 2019, 15, 73. [Google Scholar] [CrossRef]
  173. Lan, H.; Chen, C.L.; Miao, Y.; Yu, C.X.; Guo, W.W.; Xu, Q.; Deng, X.X. Fragile sites of ‘Valencia’ sweet orange (Citrus sinensis) chromosomes are related with active 45S rDNA. PLoS ONE 2016, 11, e0151512. [Google Scholar] [CrossRef]
  174. Xin, H.; Zhang, T.; Han, Y.; Wu, Y.; Shi, J.; Xi, M.; Jiang, J. Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 2018, 127, 313–321. [Google Scholar] [CrossRef] [PubMed]
  175. Islam-Faridi, M.N.; Nelson, C.D.; DiFazio, S.P.; Gunter, L.E.; Tuskan, G.A. Cytogenetic analysis of Populus trichocarpa–ribosomal DNA, telomere repeat sequence, and marker-selected BACs. Cytogenet. Genome Res. 2009, 125, 74–80. [Google Scholar] [CrossRef]
  176. Datson, P.M.; Murray, B.G. Ribosomal DNA locus evolution in Nemesia: Transposition rather than structural rearrangement as the key mechanism? Chromosome Res. 2006, 14, 845–857. [Google Scholar] [CrossRef] [PubMed]
  177. Zhou, H.C.; Waminal, N.E.; Kim, H.H. In silico mining and FISH mapping of a chromosome-specific satellite DNA in Capsicum annuum L. Genes Genom. 2019, 41, 1001–1006. [Google Scholar] [CrossRef] [PubMed]
  178. Moscone, E.A.; Scaldaferro, M.A.; Grabiele, M.; Cecchini, N.M.; Sánchez García, Y.; Jarret, R.; Daviña, J.R.; Ducasse, D.A.; Barboza, G.E.; Ehrendorfer, F. The evolution of chili peppers (Capsicum-Solanaceae): A cytogenetic perspective. Acta Hortic. 2007, 745, 137–169. [Google Scholar] [CrossRef]
  179. Ganal, M.W.; Lapitan, N.L.; Tanksley, S.D. Macrostructure of the tomato telomeres. Plant Cell 1991, 3, 87–94. [Google Scholar]
  180. Parokonny, A.S.; Kenton, A.Y.; Gleba, Y.Y.; Bennett, M.D. Genome reorganization in Nicotiana asymmetric somatic hybrids analysed by in situ hybridization. Plant J. 1992, 2, 863–874. [Google Scholar] [CrossRef]
  181. Peška, V.; Matl, M.; Mandakova, T.; Vitales, D.; Fajkus, P.; Fajkus, J.; García, S. Human-like telomeres in Zostera marina reveal a mode of transition from the plant to the human telomeric sequences. J. Exp. Bot. 2020, 71, 5786–5793. [Google Scholar] [CrossRef]
  182. Cuadrado, Á.; de Bustos, A.; Jouve, N. On the allopolyploid origin and genome structure of the closely related species Hordeum secalinum and Hordeum capense inferred by molecular karyotyping. Ann. Bot. 2017, 120, 245–255. [Google Scholar]
  183. Rocha, L.C.; Mittelmann, A.; Houben, A.; Techio, V.H. Fragile sites of 45S rDNA of Lolium multiflorum are not hotspots for chromosomal breakages induced by X-ray. Mol. Biol. Rep. 2016, 43, 659–665. [Google Scholar] [CrossRef]
  184. Maluszynska, J.; Heslop-Harrison, J.S. Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J. 1991, 1, 159–166. [Google Scholar] [CrossRef]
  185. Fonsêca, A.; Pedrosa-Harand, A. Karyotype stability in the genus Phaseolus evidenced by the comparative mapping of the wild species Phaseolus microcarpus. Genome 2013, 56, 335–343. [Google Scholar] [CrossRef]
  186. Vitales, D.; D’Ambrosio, U.; Gálvez, F.; Kovařík, A.; García, S. Third release of the plant rDNA database with updated content and information on telomere composition and sequenced plant genomes. Plant Syst. Evol. 2017, 303, 1115–1121. [Google Scholar] [CrossRef] [Green Version]
  187. Angiosperm Phylogeny Website. Available online: http://www.mobot.org/MOBOT/research/APweb/ (accessed on 9 September 2021).
  188. Cole, T.C.H.; Bachelier, J.B.; Hilger, H.H. Tracheophyte phylogeny poster—Vascular plants: Systematics and characteristics. Peer J. Prepr. 2019, 7, e2614v3. [Google Scholar]
  189. Cole, T.C.H.; Hilger, H.H.; Stevens, P. Angiosperm phylogeny poster (APP)—Flowering plant systematics. Peer J. Prepr. 2019, 7, e2320v6. [Google Scholar]
  190. Clark, J.W.; Donoghue, P.C. Whole-genome duplication and plant macroevolution. Trends Plant Sci. 2018, 23, 933–945. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  191. De Bodt, S.; Maere, S.; Van de Peer, Y. Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 2005, 20, 591–597. [Google Scholar] [CrossRef]
  192. Landis, J.B.; Soltis, D.E.; Li, Z.; Marx, H.E.; Barker, M.S.; Tank, D.C.; Soltis, P.S. Impact of whole-genome duplication events on diversification rates in angiosperms. Am. J. Bot. 2018, 105, 348–363. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  193. Guerra, M. Chromosome numbers in plant cytotaxonomy: Concepts and implications. Cytogenet. Genome Res. 2008, 120, 339–350. [Google Scholar] [CrossRef]
  194. Schubert, I.; Lysak, M.A. Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet. 2011, 27, 207–216. [Google Scholar] [CrossRef]
  195. Wang, X.; Jin, D.; Wang, Z.; Guo, H.; Zhang, L.; Wang, L.; Li, J.; Paterson, A.H. Telomere-centric genome repatterning determines recurring chromosome number reductions during the evolution of eukaryotes. New Phytol. 2015, 205, 378–389. [Google Scholar] [CrossRef]
  196. Murat, F.; Xu, J.H.; Tannier, E.; Abrouk, M.; Guilhot, N.; Pont, C.; Messing, J.; Salse, J. Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res. 2010, 20, 1545–1557. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  197. Lysak, M.A.; Mandáková, T.; Schranz, M.E. Comparative paleogenomics of crucifers: Ancestral genomic blocks revisited. Curr. Opin. Plant Biol. 2016, 30, 108–115. [Google Scholar] [CrossRef]
  198. Schweizer, D.; Loidl, J. A model for heterochromatin dispersion and the evolution of C-band patterns. Chromosome Today 1987, 9, 61–74. [Google Scholar]
  199. Charlesworth, B.; Sniegowski, P.; Stephan, W. The evolutionary dynamics of the repetitive DNA of eukaryotes. Nature 1994, 371, 215–220. [Google Scholar] [CrossRef]
  200. Cohen, S.; Houben, A.; Segal, D. Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. Plant J. 2008, 53, 1027–1034. [Google Scholar] [CrossRef] [Green Version]
  201. Navrátilová, A.; Koblížková, A.; Macas, J. Survey of extrachromosomal circular DNA derived from plant satellite repeats. BMC Plant Biol. 2008, 8, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  202. Roa, F.; Guerra, M. Distribution of 45S rDNA sites in chromosomes of plants: Structural and evolutionary implications. BMC Evol. Biol. 2012, 12, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  203. The Plant List. Available online: http://www.theplantlist.org/ (accessed on 1 January 2021).
Plants 10 02541 g001 550
Figure 1. Telomeric sequences (Arabidopsis-type repeats) in (A) Lysimachia minoricensis (Primulaceae) and (B) Anacyclus pyrethrum (Asteraceae). L. minoricensis lacks ITR repeats, whereas A. pyrethrum shows many ITR sites located at proximal and interstitial regions. Scale bars = 10 µm.
Figure 1. Telomeric sequences (Arabidopsis-type repeats) in (A) Lysimachia minoricensis (Primulaceae) and (B) Anacyclus pyrethrum (Asteraceae). L. minoricensis lacks ITR repeats, whereas A. pyrethrum shows many ITR sites located at proximal and interstitial regions. Scale bars = 10 µm.
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Figure 3. Taxonomic distribution of ITRs in the sampled lineages of seed plants. The number of recorded species is indicated for each group (orange colour). The circumscription of higher taxonomic lineages follows the hypothesis of the Angiosperm Phylogeny Website [187].
Figure 3. Taxonomic distribution of ITRs in the sampled lineages of seed plants. The number of recorded species is indicated for each group (orange colour). The circumscription of higher taxonomic lineages follows the hypothesis of the Angiosperm Phylogeny Website [187].
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Figure 4. Longitudinal distribution of ITR sites along the chromosome arm in major lineages of gymnosperms and angiosperms. The percentage of occurrence in each chromosomal region is indicated. The chromosome arm was divided into three major domains of unequal size, i.e., centromeric (c), proximal (p), and interstitial (i).
Figure 4. Longitudinal distribution of ITR sites along the chromosome arm in major lineages of gymnosperms and angiosperms. The percentage of occurrence in each chromosomal region is indicated. The chromosome arm was divided into three major domains of unequal size, i.e., centromeric (c), proximal (p), and interstitial (i).
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Figure 5. Number of ITR sites reported for the major lineages of seed plants. The range and average number of ITR signals are represented.
Figure 5. Number of ITR sites reported for the major lineages of seed plants. The range and average number of ITR signals are represented.
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Figure 6. Presence and absence of ITR sites in seed plants according to the haploid chromosome number (n) of the analysed species.
Figure 6. Presence and absence of ITR sites in seed plants according to the haploid chromosome number (n) of the analysed species.
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Table
Table 1. Longitudinal distribution of ITRs in seed plants. The percentage of occurrence in each chromosomal region is indicated. The chromosome arm was divided into three major domains of unequal size, i.e., centromeric (c), proximal (p), and interstitial (t).
Table 1. Longitudinal distribution of ITRs in seed plants. The percentage of occurrence in each chromosomal region is indicated. The chromosome arm was divided into three major domains of unequal size, i.e., centromeric (c), proximal (p), and interstitial (t).
Seed Plants (%)Gymnosperms (%)Angiosperms (%)
c21.528.120.1
p29.018.831.2
i49.553.148.7
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Maravilla, A.J.; Rosato, M.; Rosselló, J.A. Interstitial Telomeric-like Repeats (ITR) in Seed Plants as Assessed by Molecular Cytogenetic Techniques: A Review. Plants 2021, 10, 2541. https://doi.org/10.3390/plants10112541

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Maravilla AJ, Rosato M, Rosselló JA. Interstitial Telomeric-like Repeats (ITR) in Seed Plants as Assessed by Molecular Cytogenetic Techniques: A Review. Plants. 2021; 10(11):2541. https://doi.org/10.3390/plants10112541

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Maravilla, Alexis J., Marcela Rosato, and Josep A. Rosselló. 2021. "Interstitial Telomeric-like Repeats (ITR) in Seed Plants as Assessed by Molecular Cytogenetic Techniques: A Review" Plants 10, no. 11: 2541. https://doi.org/10.3390/plants10112541

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